Eur. J. Entomol. 106 (4): 583-594, 2009 | 10.14411/eje.2009.073

Bottom-up effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability

Rana M. SARFRAZ*,1, Lloyd M. DOSDALL2, Andrew B. KEDDIE1
1 Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9
2 Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada T6G 2P5

The plant stress and plant vigour hypotheses are competing paradigms pertaining to the preference and performance of herbivorous insects on their host plants. Tests of these hypotheses ideally require detailed information on aspects of soil nutrition, foliar nutrient levels and parameters of herbivore fitness, but such studies are uncommon. These hypotheses were tested using the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), reared on its host plant, Brassica napus (L.), grown in an experimental system of five nutrient regimes. Different levels of fertilizer treatments significantly affected the nutrient content of B. napus foliage and this in turn affected the preference and performance of P. xylostella. Ovipositing females discriminated among host plants grown in soils subjected to different fertilizer treatments and selected plants on which pre-imaginal survival was highest, development fastest and longevity of the next generation of adults the longest, even when food was scarce. Plants subjected to herbivory by P. xylostella responded by producing elevated levels of some nutrients (e.g., sulphur), but other nutrient levels declined in infested leaves (e.g., nitrogen). Regardless of the rate of fertilizer application, plants compensated for herbivory by increasing root mass compared to un-infested control plants; plants grown in soils receiving the optimum quantity of fertilizer developed the most robust root systems when infested. The plant stress and the plant vigour hypotheses are likely to be at the opposite ends of a continuum of responses between insects and their host plants. Our investigations indicate a complex set of interactions involving both bottom-up and top-down effects, which interact to affect host plant quality, oviposition site selection by female herbivores and the fitness of their offspring.

Keywords: Lepidoptera, Plutellidae, Plutella xylostella, diamondback moth, Brassicaceae, insect-plant interactions, plant vigour, plant stress, soil fertilizer treatments

Received: June 3, 2009; Accepted: August 13, 2009; Published: November 20, 2009

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References

  1. AOAC INTERNATIONAL 2003a: Protein (crude) in animal feed: Combustion method, AOAC official method 990.03. In: Official Methods of Analysis of AOAC International, 17th edition. Association of Official Analytical Chemists, Gaithersburg, MD, USA
  2. AOAC INTERNATIONAL 2003b: Metals and other elements in plants and pet foods: Inductively coupled plasma spectroscopic method, AOAC official method 985.01. In: Official Methods of Analysis of AOAC International, 17th edition. Association of Official Analytical Chemists, Gaithersburg, MD, USA
  3. BARKER A.M. & MACZKA C.J.M. 1996: The relationships between host selection and subsequent larval performance in three free-living gramnivorous sawflies. Ecol. Entomol. 21: 317-327 Go to original source...
  4. BELSKY A.J. 1986: Does herbivory benefit plants? A review of the evidence. Am. Nat. 127: 870-892 Go to original source...
  5. BERNER D., BLACKENHORN W.U. & KORNER C. 2005: Grasshoppers cope with low host plant quality by compensatory feeding and food selection: N limitation challenged. Oikos 111: 525-533 Go to original source...
  6. BRODBECK B.V., MIZZEL R.F., FRENCH W.J., ANDERSON P.C. & ALDRICH J.H. 1990: Amino acids as determinants of host preference for the xylem feeding leafhopper, Homalodisca coagulata (Homoptera: Cicadellidae). Oecologia 83: 338-345 Go to original source...
  7. CATES R.G., HENDERSON C.B. & REDAK R.A. 1987: Responses of the western spruce budworm to varying levels of nitrogen and terpenes. Oecologia 73: 312-316 Go to original source...
  8. CHAPMAN J.W., REYNOLDS D.R., SMITH A.D., RILEY J.R., PEDGLEY D.E. & WOIWOD I.P. 2002: High altitude migration of the diamondback moth Plutella xylostella to the U. K.: A study using radar, aerial netting, and ground trapping. Ecol. Entomol. 27: 641-650 Go to original source...
  9. CHAU A. & HEINZ K.M. 2006: Manipulating fertilization: a management tactic against Frankliniella occidentalis on potted chrysanthemum. Entomol. Exp. Appl. 120: 201-209 Go to original source...
  10. CHEN Y.Z., LIN L., WANG C.W., YEH C.C. & HWANG S.Y. 2004: Response of two Pieris (Lepidoptera: Pieridae) species to fertilization of a host plant. Zool. Stud. 43: 778-786
  11. CRAIG T.P. & OHGUSHI T. 2002: Preference and performance are correlated in spittlebug Aphrophora pectoralis on four species of willow. Ecol. Entomol. 27: 529-540 Go to original source...
  12. CRAIG T.P., ITAMI J.K. & PRICE P.W. 1989: A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70: 1691-1699 Go to original source...
  13. DELTING J.K., DYER M.I. & WINN D.T. 1979: Net photosynthesis, root respiration, and regrowth of Bouteloua gracilis following simulated grazing. Oecologia 41: 127-134. Go to original source...
  14. DENNO R.F., LARSSON S. & OLMSTEAD K.L. 1990: Role of enemy-free space and plant quality in host-plant selection by willow beetles. Ecology 7: 124-137 Go to original source...
  15. DOSDALL L.M., CLAYTON G.W., HARKER K.N., O'DONOVAN J.T. & STEVENSON F.C. 2004a: The effects of soil fertility and other agronomic factors on infestations of root maggots in canola. Agron. J. 96: 1306-1313 Go to original source...
  16. DOSDALL L.M., MASON P.G., OLFERT O., KAMINSKI L. & KEDDIE B.A. 2004b: The origins of infestations of diamondback moth, Plutella xylostella (L.), in canola in western Canada. In Endersby N.M. & Ridland P.M. (eds): The Management of Diamondback Moth and Other Crucifer Pests. Proceedings of the Fourth International Workshop, 26-29 November 2001, Melbourne. Department of Natural Resources and Environment, Melbourne, pp. 95-100
  17. FISCHER K. & FIEDLER K. 2000: Response of the copper butterfly Lycaena tityrus to increased leaf nitrogen in natural food plants: Evidence against the nitrogen limitation hypothesis. Oecologia 124: 235-241 Go to original source...
  18. FLINT H.M., NARANJO S.E., LEGGETT J.E. & HENNEBERRY T.J. 1996: Cotton water stress, arthropod dynamics, and management of Bemisia tabaci (Homoptera: Aleyrodidae). J. Econ. Entomol. 89: 1288-1300 Go to original source...
  19. FLOATE M.J.S. 1981: Effects of grazing by large herbivores on nitrogen cycling in agricultural ecosystems. In Clark F.E. & Rosswall T. (eds): Terrestrial Nitrogen Cycles. Royal Swedish Academy of Sciences, Stockholm, pp. 585-602
  20. FOX C.W. & LALONDE R.G. 1993: Host confusion and the evolution of insect diet breadths. Oikos 67: 577-581 Go to original source...
  21. GARTNER B.L. 1994: Root biomechanics and whole-plant allocation patterns: responses of tomato plants to stem flexure. J. Exp. Bot. 45: 1647-1654 Go to original source...
  22. GILBERT N. 1984: Control of fecundity in Pieris rapae. I. The problem. J. Anim. Ecol. 53: 581-588 Go to original source...
  23. GUPTA P.D. & THORSTEINSON A.J. 1960: Food plant relationship of diamondback moth (Plutella maculipennis (Curt.)). II. Sensory regulation of oviposition of the adult female. Entomol. Exp. Appl. 3: 305-314 Go to original source...
  24. HARCOURT D.G. 1957: Biology of the diamondback moth, Plutella maculipennis (Curt.) (Lepidoptera: Plutellidae), in eastern Ontario. II. Life-history, behaviour, and host relationship. Can. Entomol. 12: 554-564 Go to original source...
  25. HEINRICHS E.A. 1988: Plant Stress: Insect Interactions. Wiley & Sons, New York, 492 pp
  26. HEISSWOLF A., OBERMAIER E. & POETHKE H.J. 2005: Selection of large host plants for oviposition by a monophagous leaf beetle: Nutritional quality or enemy-free space? Ecol. Entomol. 30: 299-306 Go to original source...
  27. HERMS A.A. & MATTSON W.J. 1992: The dilemma of plants: to grow or to defend. Q. Rev. Biol. 67: 283-335 Go to original source...
  28. HOLLAND E.A., PARTON W.J., DELTING J.K. & COPPOCK D.L. 1992: Physiological responses of plant populations to herbivory and their consequences for ecosystem nutrient flow. Am. Nat. 140: 685-706 Go to original source...
  29. HUNTER M.D. & MCNEIL J.N. 1997: Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78: 977-986 Go to original source...
  30. INBAR M., DOOSTDAR H. & MAYER R.T. 2001: Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94: 228-235 Go to original source...
  31. JOERN A. & BEHMER S.T. 1998: Impact of diet quality on demographic attributes in adult grasshoppers and the nitrogen limitation hypothesis. Ecol. Entomol. 23: 174-184 Go to original source...
  32. JONES C.G. & COLEMAN J.C. 1988: Plant stress and insect behavior: Cottonwood, ozone and the feeding and oviposition preference of a beetle. Oecologia 76: 51-56 Go to original source...
  33. KORICHEVA J., LARSSON S. & HAUKIOJA E. 1998: Insect performance on experimentally stressed woody plants: A metaanalysis. Annu. Rev. Entomol. 43: 195-216 Go to original source...
  34. LARSSON S. 1989: Stressful times for the plant stress-insect performance hypothesis. Oikos 56: 277-283 Go to original source...
  35. LAVOIE B. & OBERHAUSER K.S. 2004: Compensatory feeding in Danaus plexippus (Lepidoptera: Nymphalidae) in response to variation in host plant quality. Environ. Entomol. 33: 1062-1069 Go to original source...
  36. LITTELL R.C., STROUP W.W. & FREUND R.J. 2002: SAS(R) for Linear Models, 4th ed. SAS Institute Inc., Cary, NC, USA
  37. LOUDA S.M. & COLLINGE S.K. 1992: Plant resistance to insect herbivores: A field test of the environmental stress hypothesis. Ecology 73: 153-169 Go to original source...
  38. MARAZZI C., PATRIAN B. & STADLER E. 2004: Secondary metabolites of the leaf surface affected by sulphur fertilization and perceived by the diamondback moth. Chemoecology 14: 81-86 Go to original source...
  39. MASCHINSKI J. & WHITHAM T.G. 1989: The continuum of plant responses to herbivory: The influence of plant association, nutrient availability, and timing. Am. Nat. 134: 1-19 Go to original source...
  40. MATTSON W.J. 1980: Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11: 119-161 Go to original source...
  41. MATTSON W.J. & HAACK R.A. 1987: The role of drought in outbreaks of plant-eating insects. Bioscience 37: 110-118 Go to original source...
  42. MCNAUGHTON S.J., BANYIKWA F.F. & MCNAUGHTON M.M. 1998: Root biomass and productivity in a grazing ecosystem: The Serengeti. Ecology 79: 587-592 Go to original source...
  43. MEVI-SCHUTZ J., GOVERDE M. & ERHARDT A. 2003: Effects of fertilization and elevated CO2 on larval food and butterfly nectar amino acid preference in Coenonympha pamphilus L. Behav. Ecol. Sociobiol. 54: 36-43 Go to original source...
  44. MEYER G.A. 2000: Interactive effects of soil fertility and herbivory on Brassica nigra. Oikos 88: 433-441 Go to original source...
  45. MEYER G.A. & ROOT R.B. 1996: Influence of feeding guild on insect response to host plant fertilization. Ecol. Entomol. 21: 270-278 Go to original source...
  46. MITHEN R. 1992: Leaf glucosinolate profiles and their relationship to pest and disease resistance in oilseed rape. Euphytica 63: 71-83 Go to original source...
  47. MYERS J.H. 1985: Effect of physiological condition of the host plant on the ovipositional choice of the cabbage butterfly, Pieris rapae. J. Anim. Ecol. 54: 193-204 Go to original source...
  48. MYERS J.H. & POST B.J. 1981: Plant nitrogen fluctuations of insect populations: A test with the cinnebar moth-tansy ragwort system. Oecologia 48: 151-156 Go to original source...
  49. OESTERHELD M. & MCNAUGHTON S.J. 1988: Interspecific variation in the response of Themeda triandra to defoliation: The effect of time of recovery and growth rates on compensatory growth. Oecologia 77: 181-186 Go to original source...
  50. PRICE P.W. 1991: The plant vigor hypothesis and herbivore attack. Oikos 62: 244-251 Go to original source...
  51. RAMONA W., HEIDI A., MARTIN C. & JACK S. 2005: Fertility, root reserves and cost of inducible defenses in the perennial plant Solanum carolinense. J. Chem. Ecol. 31: 2263-2288 Go to original source...
  52. REESE J.C. 1979: Interactions of allelochemicals with nutrients in herbivore food. In Rosenthal G.A. & Janzen D.H. (eds): Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York, pp. 309-320
  53. RHOADES D.F. 1979: Evolution of plant chemical defense against herbivores. In Rosenthal G.A. & Janzen D.H. (eds): Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York, pp. 3-54.
  54. SARFRAZ M., KEDDIE A.B. & DOSDALL L.M. 2005: Biological control of the diamondback moth, Plutella xylostella (L.): A review. Biocontr. Sci. Technol. 15: 763-789 Go to original source...
  55. SARFRAZ M., DOSDALL L.M. & KEDDIE B.A. 2006: Diamondback moth-host plant interactions: Implications for pest management. Crop Prot. 25: 625-639 Go to original source...
  56. SARFRAZ M., DOSDALL L.M. & KEDDIE B.A. 2007: Resistance of some cultivated Brassicaceae to infestations by Plutella xylostella (Lepidoptera: Plutellidae). J. Econ. Entomol. 100: 215-224 Go to original source...
  57. SARFRAZ M., DOSDALL L.M. & KEDDIE B.A. 2009: Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biol. Control 51: 34-41 Go to original source...
  58. SAS INSTITUTE 2004: SAS User's Guide: Statistics. SAS Institute, Cary, NC, USA
  59. SCHEIRS J. & BRUYN L.D. 2005: Plant-mediated effects of drought stress on host preference and performance of a grass miner. Oikos 108: 371-385 Go to original source...
  60. SHELTON A.M., COOLEY R.J., KROENING M.K., WILSEY W.T. & EIGENBRODE S.D. 1991: Comparative analysis of two rearing procedures for diamondback moth (Lepidoptera: Plutellidae). J. Entomol. Sci. 26: 17-26
  61. SKINNER H.R. 1996: Response of Bemisia argentifolii (Homoptera: Aleyrodidae) to water and nutrient stressed cotton. Environ. Entomol. 25: 401-406 Go to original source...
  62. SLANSKY F. JR. & FEENY P. 1977: Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol. Monogr. 47: 209-228 Go to original source...
  63. STEEL R.G.D., TORRIE J.H. & DICKEY D.A. 1997: Analysis of variance II: Multiway classifications. In Steel R.G.D., Torrie J.H. & Dickey D.A. (eds): Principles and Procedures of Statistics: A Biometrical Approach. 3rd ed. WCB/McGraw-Hill, New York, NY, pp. 204-252
  64. TALEKAR N.S. & SHELTON A.M. 1993: Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol. 38: 275-301 Go to original source...
  65. TAYLOR W.E. & BARDNER R. 1968: Effects of feeding by larvae of Phaedon cochleariae (F.) and Plutella maculipennis (Curt.) on the yield of radish and turnip plants. Ann. Appl. Biol. 62: 249-254 Go to original source...
  66. TEKELI A.S. & ATES E. 2003: Yield and its components in field pea (Pisum arvense L.) lines. J. Centr. Eur. Agric. 4: 313-317
  67. THOMPSON J.N. 1988a: Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol. Exp. Appl. 47: 3-14 Go to original source...
  68. THOMPSON J.N. 1988b: Variation in interspecific interactions. Annu. Rev. Entomol. 19: 65-87 Go to original source...
  69. TRUMBLE J.T., KOLODNY-HIRSCH D.M. & TING I.P. 1993: Plant compensation for arthropod herbivory. Annu. Rev. Entomol. 119: 38-93 Go to original source...
  70. WARING G.L. & COBB N.S. 1992: The impact of plant stress on herbivore population dynamics. In Bernays E. (ed.): InsectPlant Interactions. Vol. IV. CRC Press, Boca Raton, FL, pp. 167-187
  71. WHITE T.C.R. 1969: An index to measure weather-induced stress of trees associated with outbreaks of psyllids in Australia. Ecology 50: 905-909 Go to original source...
  72. WHITE T.C.R. 1984: The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63: 90-105 Go to original source...
  73. WILLIAMS M.A. & CRONIN J.T. 2004: Response of a gall-forming guild (Hymenoptera: Cynipidae) to stressed and vigorous prairie roses. Envir. Entomol. 33: 1052-1061 Go to original source...
  74. WILLIS A.J., ASH J.E. & GROVES R.H. 1995: The effects of herbivory by a mite, Aculus hyperici, and nutrient deficiency on growth in Hypericum species. Aust. J. Bot. 43: 305-316 Go to original source...